Purpose Large-scale processing of sensory information across regions of neocortex is poorly understood. In particular, it remains unclear whether millisecond-precise action potential timing, rather than mean spike rates, contributes to the unexcelled ability of real brains to process information. If so, a deeper understanding could accelerate the development of novel augmentative devices and genetic therapies for brain disorders, and biologically-based artificial intelligence. We hypothesized that Ca++-dependent K+ AHP channels, because of their sensitivity to preceding interspike intervals patterns, would be more important than slowly reacting K+ channels for carrying information.
Methods We used a biologically-realistic computational model of spiking neurons, representing excitatory and multiple inhibitory subtypes. Each neuron included voltage and Ca++-sensitive potassium channels (A-, M-, and AHP-type) and dynamic synapses. A recording of a 3-second spoken sentence was decomposed into 100 frequency bands, and input into a custom brain simulation of auditory A-I cortex, which was recurrently connected to two A-II association columns (total of 900,000 synapses among 3,000 neurons). Shannon information was computed for spiking patterns in response to the sentence at (1) baseline and under M-knockin/AHP-knockout, and (2) under both conditions, with 10-100% auditory noise. (figure)
Results KI/KO resulted in a loss of 8.5 bits/sec information-carrying capacity, despite identical mean spiking rates. With the addition of auditory noise, the information loss increased up to 13 bits/sec. (figure)
Conclusions The information-carrying capacity of neural tissue may depend on millisecond-precise spike timing, which in turn may depend on AHP (or similar Ca++-dependent K+) channels. In this model of auditory neocortex, loss of spike timing tremendously deteriorates (1) information-carrying capacity and (2) robustness to noise.
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